Metabolic Engineering of Plant-derived (E)-β-farnesene Synthase Genes for a Novel Type of Aphid-resistant Genetically Modified Crop Plants

Aphids are major agricultural pests that cause significant yield losses of crop plants each year.Excessive dependence on insec-ticides for long-term aphid control is undesirable because of the development of insecticide resistance,the potential negative effects on non-target organisms and environmental pollution.Transgenic crops engineered for resistance to aphids via a non-toxic mode of action could be an efficient alternative strategy.(E)-β-Farnesene (EβF) synthases catalyze the formation of EβF,which for many pest aphids is the main component of the alarm pheromone involved in the chemical communication within these species.EβF can also be synthesized by certain plants but is then normally contaminated with inhibitory compounds.Engineering of crop plants capable of synthesizing and emitting EβF could cause repulsion of aphids and also the attraction of natural enemies that use EβF as a foraging cue,thus minimizing aphid infestation.In this review,the effects of aphids on host plants,plants' defenses against aphid herbivory and the recruitment of natural enemies for aphid control in an agricultural setting are briefly introduced.Furthermore,the plant-derived EβF synthase genes cloned to date along with their potential roles in generating novel aphid resistance via genetically modified approaches are discussed.     

Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions

Aphids are important agricultural and forest pests that exhibit complex behaviors elicited by pheromonal signals. The aphid alarm pheromone--of which (E)-β-farnesene is the key (or only) component in most species--plays important roles in mediating interactions among individuals as well as multitrophic interactions among plants, aphids, and aphid natural enemies. Though many important questions remain to be answered, a large body of research has addressed various aspects of the biology, physiology, and ecology of aphid alarm pheromones. Here we review recent advances in our understanding of (a) the identity and composition of aphid alarm signals; (b) their biosynthesis and production; (c) their effects on conspecifics; (d) their role as cues for other insect species; and (e) their potential application for the management of pest organisms.     

The functional significance of E-β-Farnesene: Does it influence the populations of aphid natural enemies in the fields?

Aphids cause much damage to Chinese cabbage in northern China. Over reliance on pesticides have large environmental and human health costs that compel researchers to seek alternative management tactics for aphid control. The component of aphid alarm pheromone, E-β-Farnesene (EβF), extracted from Matricaria chamomilla L., which attracts natural enemies in the laboratory, may have significant implications for the design of cabbage aphid control strategies. The purpose of this paper is to understand the effects of EβF on natural enemies to cabbage aphid control in Chinese cabbage fields. Ladybeetles on Chinese cabbage leaves in EβF released plots and Aphidiidae in EβF released yellow traps were significantly higher than those of in controls. No significant differences were detected in the interactions of different treatments and the two years for all natural enemies. More important, lower aphid densities were found in EβF released plots. Our results suggested that the EβF extracted from M. chamomilla L. could attract natural enemies to reduce cabbage aphids in the Chinese cabbage fields.     

Soybean Aphid Response to their Alarm Pheromone E-ß-Farnesene (EBF)

When attacked by natural enemies some insect pests, including many aphid species, alert neighboring conspecifics with alarm pheromones. Cornicle secretions with pheromones benefit the attacked aphid but are costly to produce, while alarm pheromone benefits probably fall largely on alerted conspecifics. Given these variable benefits, the likelihood of a secretion may change depending on aphid density. Thus, we first hypothesized that the common alarm pheromone in aphids, E-ß-farnesene (EBF), was present in soybean aphid (Aphis glycines Matsumura) cornicle secretions and would elicit an alarm response in aphids exposed to it. Second, since aphids other than the secretor also benefit from cornicle secretions, we hypothesized that the likelihood of secretion would increase concurrently with the density of neighboring clonal conspecifics. Third, because alarm reaction behavior (e.g. feeding cessation) is probably costly, we hypothesized that alarm reaction behavior would decrease as conspecific density (i.e. alternative prey for an attacking natural enemy) increased. We found that soybean aphids 1) produce cornicle secretions using EBF as an alarm pheromone, 2) are less likely to release cornicle secretions when alone than in a small group (~10 individuals), but that the rate of secretion does not increase further with additional conspecific density, and 3) also exhibit alarm reaction behavior in response to cornicle secretions independent of aphid density. We show that soybean aphids can use their cornicle secretions to warn their neighbors of probable attack by natural enemies, but that both secretion and alarm reaction behavior does not change as density of nearby conspecifics rises above a few individuals.     

Ant attendance of the cotton aphid is beneficial for okra plants: deciphering multitrophic interactions

相似文献   

Is there any evidence that aphid alarm pheromones work as prey and host finding kairomones for natural enemies?

1. The aphid alarm pheromone (E)‐β‐farnesene (EBF) is often considered to be used by natural enemies as a prey/host finding kairomone. However, studies show opposing results, some appear to confirm an attraction of aphid natural enemies by EBF whereas others do not provide any evidence for the kairomone function of EBF. 2. To clarify if aphid natural enemies are attracted by the amounts of EBF naturally emitted by aphids, the existing literature was reviewed about EBF attractiveness to aphid natural enemies with consideration of the amounts of EBF used in the studies. 3. Thirty‐one publications that investigated the ability of EBF, aphid cornicle secretion, and attacked aphids, to attract aphid natural enemies were found. Several studies showed an attraction by EBF, but these used much higher amounts of EBF than usually emitted by aphids during a predator attack. Studies investigating EBF amounts similar to what is emitted by aphids are rare and failed to show attraction. Only two studies document an attraction of natural enemies by attacked aphids. 4. As EBF is emitted in very low amounts, not very stable, and only present after an attack, we suggest that aphid‐derived EBF is not a suitable kairomone for most natural enemy species, especially when they are able to use alternative cues. As EBF, amongst other volatiles, is also emitted by herbivore‐induced plants, we propose that natural enemies might use plant‐derived EBF as a synomone to identify aphid‐infested plants via an altered plant volatile bouquet.     

小麦蚜虫田间调查及监测技术

小麦蚜虫是世界范围内小麦生产中一类重要害虫。针对麦蚜世代历期短、繁殖力强,具有趋光、趋化及迁飞等生物学及行为习性;在田间多呈聚集分布,且麦蚜易受寄主植物抗性、天敌、气象因素及农田生态条件等生物与非生物因素影响等发生为害特点,本文阐述了我国小麦蚜虫田间调查、监测技术及防治策略,以期为我国小麦蚜虫综合防控提供基础科学支撑。     

Emission of alarm pheromone by non-preyed aphid colonies

The sesquiterpene (E)-β-farnesene (Eβf) is the primary component of the alarm pheromone of most aphid species. It is released in response to physical stress including attack by natural enemies and causes aphids to cease feeding and disperse. Eβf also acts as a kairomonal cue for aphid natural enemies. In this study, we collected the headspace volatiles released by aphid colonies of different sizes. Gas chromatography-mass spectrometry analysis demonstrated the presence of Eβf in the absence of predator attack. A quadratic relationship was found between the released ( E )-β-farnesene amounts and aphid colony size. Behavioural impact of aphid alarm pheromone towards Episyrphus balteatus female oviposition behaviour was also demonstrated in this work. These results highlight the primary role of the small but continuous release of aphid alarm pheromone in mechanisms of decision-making by aphid predators during their foraging and egg-laying behaviour.     

Aphid responses to volatile cues from turnip plants (Brassica rapa) infested with phloem-feeding and chewing herbivores

Herbivore-induced plant volatiles provide foraging cues for herbivores and for herbivores’ natural enemies. Aphids induce plant volatile emissions and also utilize plant-derived olfactory volatile cues, but the chemical ecology of aphids and other phloem-feeding insects is less extensively documented than that of chewing insects. Here, we characterize the volatile cues emitted by turnip plants (Brassica rapa) under attack by an aphid (Myzus persicae) or by the chewing lepidopteran larva Heliothis virescens. We also tested the behavioral responses of M. persicae individuals to the odors of undamaged and herbivore-damaged plants presented singly or in combination, as well as to the odor of crushed conspecifics (simulating predation). Gas chromatographic analysis of the volatile blend of infested turnips revealed distinct profiles for both aphid- and caterpillar-induced plants, with induced compounds including green-leaf alcohols, esters, and isothiocyanates. In behavioral trials, aphids exhibited increased activity in the presence of plant odors and positive attraction to undamaged turnip plants. However, aphids exhibited a strong preference for the odors of healthy versus plants subjected to herbivore damage, and neither aphid- or caterpillar-damaged plants were attractive compared to clean-air controls. Reduced aphid attraction to herbivore-infested plants may be mediated by changes in the volatile blend constituent composition, including large amounts of isothiocyanates and green-leaf volatiles or, in the case of aphid-infested plants, of the aphid alarm pheromone, (E)-β-farnesene.     

作物多样性对大豆蚜的控蚜效应

【目的】研究大豆蚜发生为害及大豆与多种作物间邻作种植对大豆蚜的控制作用,为大豆蚜的可持续综合治理提供理论依据。【方法】采用系统调查的方法,研究大豆蚜和天敌田间种群动态;通过田间罩笼、人工接蚜和释放天敌的方法,研究捕食性天敌对大豆蚜种群的控制作用;在佳木斯地区进行大豆与早熟马铃薯间作,牡丹江地区进行黄瓜-大豆-玉米、甜葫芦-大豆-玉米、烟草-大豆-香瓜、甜菜-大豆-玉米等多作物带状穿插种植模式,以单作大豆田为对照,对不同种植模式的大豆田大豆蚜与天敌进行调查,研究作物多样性对大豆蚜的控制作用。【结果】2009年6月中下旬大豆蚜开始侵入大豆田,3~5周后田间有蚜株率达到100%,大豆蚜种群发生高峰期在7月下旬至8月上旬,9月上旬在田间逐渐消失。草蛉、瓢虫和寄生蜂等为蚜虫天敌优势种;按大豆蚜与天敌数量之比700︰1,释放异色瓢虫和叶色草蛉成虫7 d后,蚜虫种群减退率分别为54.78%和78.79%;大豆与早熟马铃薯间作,在大豆蚜种群迅速增长期早熟马铃薯收获(7月20日)后第5天,豆田蚜虫天敌总数是收获前的2.6倍,与同期单作大豆田相比,间作田大豆蚜种群数量降低了51.3%。大豆与甜葫芦、香瓜、烟草和玉米等作物进行多样性间作种植,在大豆蚜田间发生高峰期,单作豆田益害比为1︰65.2,多样性种植区的大豆田益害比为1︰26~1︰42,与单作大豆田相比,间作田大豆蚜种群数量降低40.7%~83.5%。【结论】2009年大豆蚜的种群高峰期为8月3日,田间的天敌优势种类为草蛉、瓢虫和寄生蜂。早熟马铃薯与大豆间作,在大豆蚜种群迅速增长期间收获早熟马铃薯,大量蚜虫天敌转移至间作的大豆田,从而形成对大豆蚜的控制。大豆与其它经济作物间邻作,大豆田天敌昆虫与蚜虫的益害比明显提高,表明利用农田作物多样性能充分发挥自然天敌的生物控害作用。     

Aphid resistance in Brassica crops: challenges, biotechnological progress and emerging possibilities

Aphids, (Hemiptera: Aphidoidea) a nefarious insect pest of Brassicaceae members including major vegetable and oilseed crops have coevolved with their host plant and emerged as most economically important insect pest of crop Brassicas. Their atypical feeding mechanism and unusual reproductive biology made them intractable to control below economic threshold level of damage to the crops. To a large extent aphid infestation is controlled by spraying agrochemicals of systemic mode of action and rarely by biological control. Use of systemic insecticides is highly cost intensive as well poses bigger threat of their incorporation in dietary chain. Breeding for genetic resistance against aphids has not been possible owing to the non-availability of resistance source within the crossable germplasms and lack of knowledge of the genetics of the trait. Genetic engineering with insect resistant transgenes seems to be the only potential avenue to address this difficult-to-accomplish breeding objective. Some success had been achieved in terms of developing aphid resistant cultivars through genetic engineering however, commercial utilization of such crops are still awaited. Thus protection of crops against aphids necessarily requires more research to identify either more effective insecticidal transgenes or biological phenomenon that can usher to new mechanism of resistance. The present review is an attempt to highlight the current status and possible avenues to develop aphid resistance in Brassicaceae crops.     

Aphid alarm pheromone as a cue for ants to locate aphid partners

The mutualistic relationships that occur between myrmecophilous aphids and ants are based on the rich food supply that honeydew represents for ants and on the protection they provide against aphid natural enemies. While aphid predators and parasitoids actively forage for oviposition sites by using aphid semiochemicals, scouts of aphid-tending ant species would also benefit from locating honeydew resources by orienting toward aphid pheromone sources. The present study aims to provide additional information on the use of Aphis fabae alarm pheromone, i.e. (E)-β-farnesene (EβF), by ant scouts. The perception and behavioral impact of EβF on Lasius niger were investigated using electroantennography and two bio-assays measuring their attraction and orientation towards aphid semiochemicals. Pronounced electrical depolarizations were observed from L. niger scout antennae to stimulations of A. fabae alarm pheromone, while other sesquiterpenes elicited weak or no responses. L. niger scouts were significantly attracted toward EβF in a four-arm olfactometer, as well as in an two-choice bioassay. These laboratory results suggest for the first time that low amounts of aphid alarm pheromone can be used by L. niger scouts as a cue indicating the presence of aphid colonies and could therefore mediate the aphid-ant partnership in the field.     

Preceding crop affects soybean aphid abundance and predator–prey dynamics in soybean

Crop rotations alter the soil environment and physiology of the subsequent crop in ways that may affect the abundance of herbivores and their natural enemies. Soybean aphids are a consistent pest of soybean throughout North America, but little work has focused on how preceding crops may affect pest–predator dynamics. In a replicated experiment over three years, we examined how two preceding crops (spring wheat or an oat/pea mixture) affected seasonal soybean aphid pressure and the ratio of aphids to their predator community. Peak aphid populations were reduced by 40% and 75% in years 1 and 2 by planting spring wheat before soybeans (relative to the oat–pea mixture). Aphid densities were unaffected by preceding crop in the third year of study (aphids were at threshold in this year). Predators responded positively to aphid population increases and were unaffected by preceding crops. Additional research on how crop rotations can be used as a tool to manage soybean aphids warrants further attention.     

Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, shape Rhopalosiphum maidis

When maize plants, Zea mays L., are mechanically damaged and the damaged sites are treated with caterpillar regurgitant, the plants will release a specific blend of volatiles. It is known that these volatiles can be attractive to natural enemies of herbivores. We hypothesise that the plant volatiles constitute part of the induced plant defence and that herbivores will be affected by the odours as well. In laboratory and semi-field studies this hypothesis was tested for the aphid Rhopalosiphum maidis (Fitch) (Rhynchota, Sternorrhyncha, Aphididae).In a Y-tube olfactometer significantly more aphids chose the odour of healthy, undamaged maize seedlings when tested against clean air or plants treated with regurgitant. Clean air was chosen more often when tested next to the odour of treated plants. This apparently repellent effect of the odour of treated plants was significant for winged aphids, but not for the wingless aphids.In field experiments aphids were released in the centre of circles of eight potted maize plants. Four plants in each circle were damaged and treated with caterpillar regurgitant while the other plants were left unharmed. At different intervals after aphid release, the number of aphids was counted on each plant. Significantly fewer winged and wingless aphids were found back on treated plants than on healthy plants.We suggest that herbivores may be repelled by the odours because they could indicate that: 1) the plant has initiated the production of toxic compounds; 2) potential competitors are present on the plant; 3) the plant is attractive to parasitoids and predators. Aphids may be particularly sensitive to induced maize volatiles because one of the major compounds emitted by the plant is (E)--farnesene, which is a common alarm pheromone for aphids. Collections and analyses of the odours emitted by crushed R. maidis confirmed that it too emits (E)--farnesene when stressed. The results are discussed in context of plant defence strategies and their possible exploitation for the control of pest insects.     

Fitness trade-off in peach-potato aphids (Myzus persicae) between insecticide resistance and vulnerability to parasitoid attack at several spatial scales

Insecticide-resistant clones of the peach-potato aphid, Myzus persicae (Sulzer), have previously been shown to have a reduced response to aphid alarm pheromone compared to susceptible ones. The resulting vulnerability of susceptible and resistant aphids to attack by the primary endoparasitoid, Diaeretiella rapae (McIntosh), was investigated across three spatial scales. These scales ranged from aphids confined on individual leaves exposed to single female parasitoids, to aphids on groups of whole plants exposed to several parasitoids. In all experiments, significantly fewer aphids from insecticide-susceptible clones became parasitised compared to insecticide-resistant aphids. Investigations of aphid movement showed at the largest spatial scale that more susceptible aphids than resistant aphids moved from their inoculation leaves to other leaves on the same plant after exposure to parasitoids. The findings imply that parasitoids, and possibly other natural enemies, can influence the evolution and dynamics of insecticide resistance through pleiotropic effects of resistance genes on important behavioural traits.     

The role of olfaction in aphid host location

Aphids are major economic pests of many of the worlds' crops, causing damage directly by feeding and by acting as vectors for plant viruses. By understanding how aphids locate their host plants, it may become possible to develop new means of controlling populations by taking advantage of these natural host location/nonhost avoidance behaviours. Aphids have also become important model organisms in the study of insect–plant interactions and an improved understanding of host location in aphids could yield insights into the behaviour and ecology of other insect orders. The use of olfaction by host‐seeking aphids is well documented and, in recent years, considerable information has been gained on how volatiles can encode host identity and suitability, as well as the specific behaviours they elicit from aphids. The purpose of this review is to highlight the major findings on how aphids respond behaviourally to volatile compounds and how they can use them to locate their host plants and avoid unsuitable hosts.     

Alarm pheromone emission by pea aphid, Acyrthosiphon pisum, clones under predation by lacewing larvae

Genetic variation in anti-predator traits has been shown for a variety of species. Aphid alarm pheromone, ( E )-β-farnesene, is released by attacked aphids and causes a variety of behavioral defense reactions in the signal receivers. In pea aphids, Acyrthosiphon pisum Harris (Homoptera: Aphididae), ( E )-β-farnesene mediates the production of winged offspring in the presence of natural enemies. While variation in the propensity for pea aphids to produce winged offspring is well-documented, little quantitative information is available about clonal differences in ( E )-β-farnesene emission or the amount of alarm pheromone released in aphid colonies. We tested the wing induction response of four clones when attacked by a predatory lacewing larva, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae), and found that three of the four clones increased the proportion of winged offspring under predator attack. We then investigated the emission of aphid alarm pheromone of these clones of pea aphid under attack. Alarm pheromone emission in aphid colonies of initially 25 adults varied from 81.2 to 10 851.0 ng per aphid colony over 24 h. There were no differences between clones in total emission or in emission per consumption event. These results show that there is substantial variability in alarm pheromone emission within clones and that the propensity to produce winged offspring in some clones is not a simple function of the propensity of alarm pheromone production in these clones.     

Alarm pheromone mediates production of winged dispersal morphs in aphids

The aphid alarm pheromone ( E )- β -farnesene (EBF) is the major example of defence communication in the insect world. Released when aphids are attacked by predators such as ladybirds or lacewing larvae, aphid alarm pheromone causes behavioural reactions such as walking or dropping off the host plant. In this paper, we show that the exposure to alarm pheromone also induces aphids to give birth to winged dispersal morphs that leave their host plants. We first demonstrate that the alarm pheromone is the only volatile compound emitted from aphid colonies under predator attack and that emission is proportional to predator activity. We then show that artificial alarm pheromone induces groups of aphids but not single individuals to produce a higher proportion of winged morphs among their offspring. Furthermore, aphids react more strongly to the frequency of pheromone release than the amount of pheromone delivered. We suggest that EBF leads to a 'pseudo crowding' effect whereby alarm pheromone perception causes increased walking behaviour in aphids resulting in an increase in the number of physical contacts between individuals, similar to what happens when aphids are crowded. As many plants also produce EBF, our finding suggests that aphids could be manipulated by plants into leaving their hosts, but they also show that the context-dependence of EBF-induced wing formation may hinder such an exploitation of intraspecific signalling by plants.     

Infection with an insect virus affects olfactory behaviour and interactions with host plant and natural enemies in an aphid

Aphid ecology and population dynamics are affected by a series of factors including behavioural responses to ecologically relevant chemical cues, capacity for population growth, and interactions with host plants and natural enemies. Using the aphid Rhopalosiphum padi (L.) (Homoptera: Aphididae), we showed that these factors were affected by infection with Rhopalosiphum padi virus (RhPV). Uninfected aphids were attracted to odour of uninfected aphids on the host plant, an aggregation mechanism. However, infected aphids were not attracted, and neither infected nor uninfected aphids were attracted to infected aphids on the plant. Infected aphids did not respond to methyl salicylate, a cue denoting host suitability. Infected aphids were more behaviourally sensitive to aphid alarm pheromone, and left the host plant more readily in response to it. RhPV reduced the lifespan and population growth rate of the aphid. The predacious ladybird, Coccinella septempunctata (L.) (Coleoptera: Coccinellidae), consumed more infected aphids than uninfected aphids in a 24‐h period, and the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae) attacked more infected than uninfected aphids. However, the proportion of mummies formed was lower with infected aphids. The results represent further evidence that associated organisms can affect the behaviour and ecology of their aphid hosts.     

The influence of Lasius neoniger (Hymenoptera: Formicidae) on population growth and biomass of Aphis glycines (Hemiptera: Aphididae) in soybeans

In the United States, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), are often tended by the aphid-tending ant, Lasius neoniger Emery (Hymenoptera: Formicidae). In this study, we examined the effects of tending by ants on the density and biomass of soybean aphids on soybeans in Kentucky. We performed cage studies that limited access by ants and/or natural enemies. We used a split-plot design with natural enemy access as the main plot and ant attendance as the sub plot. We found that natural enemy access negatively affected aphid population density in the presence of tending ants, seen as a three- to four-fold increase in aphid density when natural enemies were excluded. In addition, we found that ant tending positively affected aphid biomass, both when natural enemies were given access to aphids or when natural enemies were excluded, seen by a two-fold increase in aphid biomass when ants tended aphids, both in the presence or absence of natural enemies. Biomass accumulation is seen as an important measurement for assessing aphid performance, and we argue that aphid-tending by ants can have an influence on natural field populations of soybean aphids. Agronomic practices that affect ant abundance in soybeans may influence the performance and hence pest outbreaks for this economically important pest.